Anti-α-internexin autoantibody from neuropsychiatric lupus induce cognitive damage via inhibiting axonal elongation and promote neuron apoptosis

PLoS ONE

Volumn 5, Issue 6, 2010, Pages

  Lu, Xiao ye ^a   Chen, Xiao xiang ^a   Huang, Li dong ^a   Zhu, Chang qing ^b   Gu, Yue ying ^a   Ye, Shuang ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERNEXIN; ALPHA INTERNEXIN ANTIBODY; AUTOANTIBODY; AUTOANTIGEN; UNCLASSIFIED DRUG; ALPHA-INTERNEXIN; INTERMEDIATE FILAMENT PROTEIN;

ADULT; AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY TITER; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN DAMAGE; BRAIN NERVE CELL; CEREBROSPINAL FLUID LEVEL; COGNITIVE DEFECT; CONTROLLED STUDY; EMBRYO; FEMALE; HIPPOCAMPUS; HISTOPATHOLOGY; HUMAN; IMMUNIZATION; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; MOUSE; NERVE CELL; NERVE CELL LESION; NERVE FIBER GROWTH; NEUROFILAMENT; NONHUMAN; PATHOPHYSIOLOGY; PROTEOMICS; RAT; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; C57BL MOUSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; NERVE FIBER; PATHOLOGY;

ANIMALIA; MURINAE;

ANIMALS; APOPTOSIS; AUTOANTIBODIES; AXONS; COGNITION DISORDERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HUMANS; INTERMEDIATE FILAMENT PROTEINS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, INBRED C57BL; NEURONS;

EID: 77956207014     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011124     Document Type: Article

References (88)

1. Sherer Y, Gorstein A, Fritzler MJ, Shoenfeld Y (2004) Autoantibody explosion in systemic lupus erythematosus: more than 100 different antibodies found in SLE patients. Semin Arthritis Rheum 34: 501-537.
2. Sanna G, Bertolaccini ML, Cuadrado MJ, Khamashta MA, Hughes GR (2003) Central nervous system involvement in the antiphospholipid (Hughes) syndrome. Rheumatology (Oxford) 42: 200-213.
3. Sanna G, Piga M, Terryberry JW, Peltz MT, Giagheddu S, et al. (2000) Central nervous system involvement in systemic lupus erythematosus: cerebral imaging and serological profile in patients with and without overt neuropsychiatric manifestations. Lupus 9: 573-583.
4. Stinton LM, Eystathioy T, Selak S, Chan EK, Fritzler MJ (2004) Autoantibodies to protein transport and messenger RNA processing pathways: endosomes, lysosomes, Golgi complex, proteasomes, assemblyosomes, exosomes, and GW bodies. Clin Immunol 110: 30-44.
5. Bhanji RA, Eystathioy T, Chan EK, Bloch DB, Fritzler MJ (2007) Clinical and serological features of patients with autoantibodies to GW/P bodies. Clin Immunol 125: 247-256.
6. Afeltra A, Garzia P, Mitterhofer AP, Vadacca M, Galluzzo S, et al. (2003) Neuropsychiatric lupus syndromes: relationship with antiphospholipid antibod- ies. Neurology 61: 108-110.
7. Diamond B, Volpe B (2003) On the track of neuropsychiatric lupus. Arthritis Rheum 48: 2710-2712.
8. Fragoso-Loyo H, Cabiedes J, Orozco-Narvaez A, Davila-Maldonado L, AtishaFregoso Y, et al. (2008) Serum and cerebrospinal fluid autoantibodies in patients with neuropsychiatric lupus erythematosus. Implications for diagnosis and pathogenesis. PLoS One 3: e3347.
9. Zhang J, Jacobi AM, Wang T, Berlin R, Volpe BT, et al. (2009) Polyreactive autoantibodies in systemic lupus erythematosus have pathogenic potential. J Autoimmun 33: 270-274.
10. Trysberg E, Nylen K, Rosengren LE, Tarkowski A (2003) Neuronal and astrocytic damage in systemic lupus erythematosus patients with central nervous system involvement. Arthritis Rheum 48: 2881-2887.
11. Zameer A, Hoffman SA (2004) B and T cells in the brains of autoimmune mice. J Neuroimmunol 146: 133-139.
12. Sidor MM, Sakic B, Malinowski PM, Ballok DA, Oleschuk CJ, et al. (2005) Elevated immunoglobulin levels in the cerebrospinal fluid from lupus-prone mice. J Neuroimmunol 165: 104-113.
13. Ma X, Foster J, Sakic B (2006) Distribution and prevalence of leukocyte phenotypes in brains of lupus-prone mice. J Neuroimmunol 179: 26-36.
14. Lawrence DA, Bolivar VJ, Hudson CA, Mondal TK, Pabello NG (2007) Antibody induction of lupus-like neuropsychiatric manifestations. J Neuroimmunol 182: 185-194.
15. Sled JG, Spring S, van Eede M, Lerch JP, Ullal S, et al. (2009) Time course and nature of brain atrophy in the MRL mouse model of central nervous system lupus. Arthritis Rheum 60: 1764-1774.
16. (1999) The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 42: 599-608.
17. Sabbadini MG, Manfredi AA, Bozzolo E, Ferrario L, Rugarli C, et al. (1999) Central nervous system involvement in systemic lupus erythematosus patients without overt neuropsychiatric manifestations. Lupus 8: 11-19.
18. Ainiala H, Loukkola J, Peltola J, Korpela M, Hietaharju A (2001) The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus. Neurology 57: 496-500.
19. Monastero R, Bettini P, Del Zotto E, Cottini E, Tincani A, et al. (2001) Prevalence and pattern of cognitive impairment in systemic lupus erythematosus patients with and without overt neuropsychiatric manifestations. J Neurol Sci 184: 33-39.
20. Diamond B, Kowal C, Huerta PT, Aranow C, Mackay M, et al. (2006) Immunity and acquired alterations in cognition and emotion: lessons from SLE. Adv Immunol 89: 289-320.
21. Hoffman SA, Arbogast DN, Ford PM, Shucard DW, Harbeck RJ (1987) Brain- reactive autoantibody levels in the sera of ageing autoimmune mice. Clin Exp Immunol 70: 74-83.
22. Shoenfeld Y, Nahum A, Korczyn AD, Dano M, Rabinowitz R, et al. (2003) Neuronal-binding antibodies from patients with antiphospholipid syndrome induce cognitive deficits following intrathecal passive transfer. Lupus 12: 436-442.
23. Shoenfeld Y, Twig G, Katz U, Sherer Y (2008) Autoantibody explosion in antiphospholipid syndrome. J Autoimmun 30: 74-83.
24. Tin SK, Xu Q, Thumboo J, Lee LY, Tse C, et al. (2005) Novel brain reactive autoantibodies: prevalence in systemic lupus erythematosus and association with psychoses and seizures. J Neuroimmunol 169: 153-160.
25. Diamond B, Volpe BT (2006) Antibodies and brain disease: a convergence of immunology and physiology. PLoS Med 3: e498.
26. Sasajima T, Watanabe H, Sato S, Sato Y, Ohira H (2006) Anti-triosephosphate isomerase antibodies in cerebrospinal fluid are associated with neuropsychiatric lupus. J Neuroimmunol 181: 150-156.
27. Lefranc D, Launay D, Dubucquoi S, de Seze J, Dussart P, et al. (2007) Characterization of discriminant human brain antigenic targets in neuropsy- chiatric systemic lupus erythematosus using an immunoproteomic approach. Arthritis Rheum 56: 3420-3432.
28. Huizinga TW, Diamond B (2008) Lupus and the central nervous system. Lupus 17: 376-379.
29. Colasanti T, Delunardo F, Margutti P, Vacirca D, Piro E, et al. (2009) Autoantibodies involved in neuropsychiatric manifestations associated with systemic lupus erythematosus. J Neuroimmunol 212: 3-9.
30. Lee JY, Huerta PT, Zhang J, Kowal C, Bertini E, et al. (2009) Neurotoxic autoantibodies mediate congenital cortical impairment of offspring in maternal lupus. Nat Med 15: 91-96.
31. DeGiorgio LA, Konstantinov KN, Lee SC, Hardin JA, Volpe BT, et al. (2001) A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat Med 7: 1189-1193.
32. Kowal C, DeGiorgio LA, Nakaoka T, Hetherington H, Huerta PT, et al. (2004) Cognition and immunity; antibody impairs memory. Immunity 21: 179-188.
33. Kowal C, Degiorgio LA, Lee JY, Edgar MA, Huerta PT, et al. (2006) Human lupus autoantibodies against NMDA receptors mediate cognitive impairment. Proc Natl Acad Sci U S A 103: 19854-19859.
34. Huerta PT, Kowal C, DeGiorgio LA, Volpe BT, Diamond B (2006) Immunity and behavior: antibodies alter emotion. Proc Natl Acad Sci U S A 103: 678-683.
35. Katzav A, Ben-Ziv T, Chapman J, Blank M, Reichlin M, et al. (2008) Anti-P ribosomal antibodies induce defect in smell capability in a model of CNS -SLE (depression). J Autoimmun 31: 393-398.
36. Matus S, Burgos PV, Bravo-Zehnder M, Kraft R, Porras OH, et al. (2007) Antiribosomal-P autoantibodies from psychiatric lupus target a novel neuronal surface protein causing calcium influx and apoptosis. J Exp Med 204: 3221-3234.
37. Nived O, Sturfelt G, Liang MH, De Pablo P (2003) The ACR nomenclature for CNS lupus revisited. Lupus 12: 872-876.
38. Kozora E, Ellison MC, West S (2004) Reliability and validity of the proposed American College of Rheumatology neuropsychological battery for systemic lupus erythematosus. Arthritis Rheum 51: 810-818.
39. Lu X, Gu Y, Wang Y, Chen S, Ye S (2008) Prognostic factors of lupus myelopathy. Lupus 17: 323-328.
40. Lu X, Zhu C, Qian J, Chen X, Ye S, Gu Y (2010) Intrathecal cytokine and chemokine profiling in neuropsychiatric lupus or lupus complicated with central nervous system infection. Lupus 2010 Feb 23.
41. Rajasalu T, Teesalu K, Janmey PA, Uibo R (2004) Demonstration of natural autoantibodies against the neurofilament protein alpha-internexin in sera of patients with endocrine autoimmunity and healthy individuals. Immunol Lett 94: 153-160.
42. Watanabe H, Seino T, Sato Y (2004) Antibodies to triosephosphate isomerase in patients with neuropsychiatric lupus. Biochem Biophys Res Commun 321: 949-953.
43. Lennon VA, Wingerchuk DM, Kryzer TJ, Pittock SJ, Lucchinetti CF, et al. (2004) A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 364: 2106-2112.
44. D'Hooge R, De Deyn PP (2001) Applications of the Morris water maze in the study of learning and memory. Brain Res Brain Res Rev 36: 60-90.
45. Zhang WW, Song MK, Cui YY, Wang H, Zhu L, et al. (2008) Differential neuropsychopharmacological influences of naturally occurring tropane alkaloids anisodamine versus scopolamine. Neurosci Lett 443: 241-245.
46. Nie BM, Jiang XY, Cai JX, Fu SL, Yang LM, et al. (2008) Panaxydol and panaxynol protect cultured cortical neurons against Abeta25-35-induced toxicity. Neuropharmacology 54: 845-853.
47. Nie BM, Yang LM, Fu SL, Jiang XY, Lu PH, et al. (2006) Protective effect of panaxydol and panaxynol on sodium nitroprusside-induced apoptosis in cortical neurons. Chem Biol Interact 160: 225-231.
48. Chien CL, Liem RK (1994) Characterization of the mouse gene encoding the neuronal intermediate filament protein alpha-internexin. Gene 149: 289-292.
49. Chan SO, Chiu FC (1996) The 66-kDa neurofilament protein (NF-66): sequence analysis and evolution. Neurochem Res 21: 449-455.
50. Chan SO, Peng D, Chiu FC (1997) Heterogeneous expression of neurofilament proteins in forebrain and cerebellum during development: clinical implications for spinocerebellar ataxia. Brain Res 775: 107-118.
51. Kaplan MP, Chin SS, Fliegner KH, Liem RK (1990) Alpha-internexin, a novel neuronal intermediate filament protein, precedes the low molecular weight neurofilament protein (NF-L) in the developing rat brain. J Neurosci 10: 2735-2748.
52. Chien CL, Mason CA, Liem RK (1996) alpha-Internexin is the only neuronal intermediate filament expressed in developing cerebellar granule neurons. J Neurobiol 29: 304-318.
53. Narendran A, Hoffman SA (1989) Characterization of brain-reactive autoan- tibodies in murine models of systemic lupus erythematosus. J Neuroimmunol 24: 113-123.
54. Maric D, Millward JM, Ballok DA, Szechtman H, Denburg JA, et al. (2001) Neurotoxic properties of cerebrospinal fluid from behaviorally impaired autoimmune mice. Brain Res 920: 183-193.
55. Arabo A, Costa O, Tron F, Caston J (2005) Spatial and motor abilities during the course of autoimmune disease in (NZW x BXSB)F1 lupus-prone mice. Behav Brain Res 165: 126-137.
56. Sakic B, Hanna SE, Millward JM (2005) Behavioral heterogeneity in an animal model of neuropsychiatric lupus. Biol Psychiatry 57: 679-687.
57. Mondal TK, Saha SK, Miller VM, Seegal RF, Lawrence DA (2008) Autoantibody-mediated neuroinflammation: pathogenesis of neuropsychiatric systemic lupus erythematosus in the NZM88 murine model. Brain Behav Immun 22: 949-959.
58. Kimura A, Sakurai T, Tanaka Y, Hozumi I, Takahashi K, et al. (2008) Proteomic analysis of autoantibodies in neuropsychiatric systemic lupus erythematosus patient with white matter hyperintensities on brain MRI. Lupus 17: 16-20.
59. Robbins ML, Kornguth SE, Bell CL, Kalinke T, England D, et al. (1988) Antineurofilament antibody evaluation in neuropsychiatric systemic lupus erythematosus. Combination with anticardiolipin antibody assay and magnetic resonance imaging. Arthritis Rheum 31: 623-631.
60. Senecal JL, Rauch J (1988) Hybridoma lupus autoantibodies can bind major cytoskeletal filaments in the absence of DNA-binding activity. Arthritis Rheum 31: 864-875.
61. Pachter JS, Liem RK (1985) alpha-Internexin, a 66-kD intermediate filament- binding protein from mammalian central nervous tissues. J Cell Biol 101: 1316-1322.
62. Fliegner KH, Ching GY, Liem RK (1990) The predicted amino acid sequence of alpha-internexin is that of a novel neuronal intermediate filament protein. EMBO J 9: 749-755.
63. Ho CL, Liem RK (1996) Intermediate filaments in the nervous system: implications in cancer. Cancer Metastasis Rev 15: 483-497.
64. Lee MK, Cleveland DW (1994) Neurofilament function and dysfunction: involvement in axonal growth and neuronal disease. Curr Opin Cell Biol 6: 34-40.
65. Yuan A, Rao MV, Sasaki T, Chen Y, Kumar A, et al. (2006) Alpha-internexin is structurally and functionally associated with the neurofilament triplet proteins in the mature CNS. J Neurosci 26: 10006-10019.
66. Williams RC, Jr., Sugiura K, Tan EM (2004) Antibodies to microtubule- associated protein 2 in patients with neuropsychiatric systemic lupus erythema- tosus. Arthritis Rheum 50: 1239-1247.
67. Senecal JL, Raymond Y (2004) The pathogenesis of neuropsychiatric manifestations in systemic lupus erythematosus: a disease in search of autoantibodies, or autoantibodies in search of a disease? J Rheumatol 31: 2093-2098.
68. Fliegner KH, Kaplan MP, Wood TL, Pintar JE, Liem RK (1994) Expression of the gene for the neuronal intermediate filament protein alpha-internexin coincides with the onset of neuronal differentiation in the developing rat nervous system. J Comp Neurol 342: 161-173.
69. Lee MK, Cleveland DW (1996) Neuronal intermediate filaments. Annu Rev Neurosci 19: 187-217.
70. Arnold SE, Trojanowski JQ (1996) Human fetal hippocampal development: II. The neuronal cytoskeleton. J Comp Neurol 367: 293-307.
71. Athlan ES, Mushynski WE (1997) Heterodimeric associations between neuronal intermediate filament proteins. J Biol Chem 272: 31073-31078.
72. Cairns NJ, Grossman M, Arnold SE, Burn DJ, Jaros E, et al. (2004) Clinical and neuropathologic variation in neuronal intermediate filament inclusion disease. Neurology 63: 1376-1384.
73. Ching GY, Chien CL, Flores R, Liem RK (1999) Overexpression of alpha- internexin causes abnormal neurofilamentous accumulations and motor coordination deficits in transgenic mice. J Neurosci 19: 2974-2986.
74. Ching GY, Liem RK (1991) Structure of the gene for the neuronal intermediate filament protein alpha-internexin and functional analysis of its promoter. J Biol Chem 266: 19459-19468.
75. Lee MK, Xu Z, Wong PC, Cleveland DW (1993) Neurofilaments are obligate heteropolymers in vivo. J Cell Biol 122: 1337-1350.
76. Beaulieu JM, Robertson J, Julien JP (1999) Interactions between peripherin and neurofilaments in cultured cells: disruption of peripherin assembly by the NF-M and NF-H subunits. Biochem Cell Biol 77: 41-45.
77. Shea TB, Beermann ML (1999) Neuronal intermediate filament protein alpha- internexin facilitates axonal neurite elongation in neuroblastoma cells. Cell Motil Cytoskeleton 43: 322-333.
78. Chien CL, Liu TC, Ho CL, Lu KS (2005) Overexpression of neuronal intermediate filament protein alpha-internexin in PC12 cells. J Neurosci Res 80: 693-706.
79. Barry DM, Millecamps S, Julien JP, Garcia ML (2007) New movements in neurofilament transport, turnover and disease. Exp Cell Res 313: 2110-2120.
80. Cairns NJ, Uryu K, Bigio EH, Mackenzie IR, Gearing M, et al. (2004) alpha- Internexin aggregates are abundant in neuronal intermediate filament inclusion disease (NIFID) but rare in other neurodegenerative diseases. Acta Neuropathol 108: 213-223.
81. Lalonde R, Strazielle C (2003) Neurobehavioral characteristics of mice with modified intermediate filament genes. Rev Neurosci 14: 369-385.
82. Lariviere RC, Julien JP (2004) Functions of intermediate filaments in neuronal development and disease. J Neurobiol 58: 131-148.
83. Alarcon-Segovia D, Ruiz-Arguelles A, Fishbein E (1978) Antibody to nuclear ribonucleoprotein penetrates live human mononuclear cells through Fc receptors. Nature 271: 67-69.
84. Alarcon-Segovia D, Ruiz-Arguelles A, Llorente L (1996) Broken dogma: penetration of autoantibodies into living cells. Immunol Today 17: 163-164.
85. Zack DJ, Stempniak M, Wong AL, Taylor C, Weisbart RH (1996) Mechanisms of cellular penetration and nuclear localization of an anti-double strand DNA autoantibody. J Immunol 157: 2082-2088.
86. Williams RC, Jr., Peen E (1999) Apoptosis and cell penetration by autoantibody may represent linked processes. Clin Exp Rheumatol 17: 643-647.
87. Cleveland DW, Rothstein JD (2001) From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2: 806-819.
88. Robertson J, Kriz J, Nguyen MD, Julien JP (2002) Pathways to motor neuron degeneration in transgenic mouse models. Biochimie 84: 1151-1160.